Download Enigmatic Cranial Superstructures Among Chamorro Ancestors

THE ANATOMICAL RECORD 297:1009–1021 (2014)
Enigmatic Cranial Superstructures
Among Chamorro Ancestors From the
Mariana Islands: Gross Anatomy and
Microanatomy
GARY M. HEATHCOTE,1* TIMOTHY G. BROMAGE,2,3 VINCENT J. SAVA,4
DOUGLAS B. HANSON,5 AND BRUCE E. ANDERSON6
1
Department of Anthropology, St. Thomas University, Fredericton, New Brunswick,
Canada
2
Hard Tissue Research Unit, Department of Biomaterials and Biomimetics, New York
University College of Dentistry, New York, New York
3
Department of Basic Science and Craniofacial Biology, New York University College of
Dentistry, New York, New York
4
JPAC Central Identification Laboratory, Joint Base Pearl Harbor-Hickam, Pearl Harbor,
Hawaii
5
The Forsyth Institute, Cambridge, Massachusetts
6
School of Anthropology, University of Arizona, Tucson, Arizona
ABSTRACT
This study focuses on the gross anatomy, anatomic relations, microanatomy, and the meaning of three enigmatic, geographically patterned,
and quasi-continuous superstructures of the posterior cranium. Collectively known as occipital superstructures (OSSs), these traits are the occipital torus tubercle (TOT), retromastoid process (PR), and posterior
supramastoid tubercle (TSP). When present, TOT, PR, and TSP develop
at posterior cranial attachment sites of the upper trapezius, superior
oblique, and sternocleidomastoid muscles, respectively. Marked expression and co-occurrence of these OSSs are virtually circumscribed within
Oceania and reach highest recorded frequencies in protohistoric Chamorros (CHamoru) of the Mariana Islands. Prior to undertaking scanning
electron microscopy (SEM) work, our working multifactorial model for
OSS development was that early-onset, long-term, and chronic activityrelated microtrauma at enthesis sites led to exuberant reactive or reparative responses in a substantial minority of genetically predisposed (and
mostly male) individuals. SEM imaging, however, reveals topographic
patterning that questions, but does not negate, activity induction of these
superstructures. Although OSSs appear macroscopically as relatively
large and discrete phenomena, SEM findings reveal a unique, widespread, and seemingly systemic distribution of structures over the occipital surface that have the appearance of OSS microforms. Nevertheless,
apparent genetic underpinnings, anatomic relationships with muscle
entheses, and positive correlation of OSS development with humeral
robusticity continue to suggest that these superstructures have potential
to at once bear witness to Chamorro population history and inform osteo-
The authors dedicate this paper to the family of their colleague, friend, exceptional scholar, and exceptionally good man,
the late Douglas B. Hanson.
Grant sponsors: NSF and Max Planck (T.G.B.); NIEHS
(D.B.H.); College of Liberal Arts and Social Sciences, University
of Guam (G.M.H.).
C 2014 WILEY PERIODICALS, INC.
V
*Correspondence to: Gary M. Heathcote, Department of
Anthropology, St. Thomas University, Fredericton, NB E3B
5G3, Canada. E-mail: [email protected]
Revised 4 February 2014; Accepted 19 February 2014.
DOI 10.1002/ar.22920
Published online 18 April 2014 in Wiley Online Library
(wileyonlinelibrary.com).
1010
HEATHCOTE ET AL.
biographical constructions of chronic activity patterns in individuals bearing them. Further work is outlined that would illuminate the proximate
C 2014
and ultimate meanings of OSS. Anat Rec, 297:1009–1021, 2014. V
Wiley Periodicals, Inc.
Key words: Chamorros; occipital torus tubercle; retromastoid
process; posterior supramastoid tubercle; entheses; functional anatomy; SEM survey
INTRODUCTION
Cranial superstructures refer to muscle and tendon
markings, such as crests, tubercles, tuberosities, and
processes, macroscopically observed on the external surface of the braincase (Weidenreich, 1940). We focus on
three superstructures of the posterior cranium: (1)
tubercle development on the torus occipitalis (occipital
torus tubercle [TOT]), (2) processus retromastoideus (retromastoid process [PR]), and (3) tuberculum supramastoideum posterius (posterior supramastoid tubercle
[TSP]), all of which are encountered more frequently
among anatomically modern humans indigenous to Oceania (Pacific Islands and Australia) than in non-Oceanic
populations. Among the indigenous people of the
Mariana Islands (Chamorros or CHamoru), who lived
during the overlapping Latte (AD 1000–1700) and Early
Historic (AD 1521–1700) Periods (Moore, 2002), these
superstructures occur at very highest frequencies and
strongest degrees of expression (Heathcote et al., 2012b;
Heathcote et al., forthcoming). Few morphological traits
of the human skeleton are similarly geographically circumscribed such that they are virtual phenotypic
markers of regional populations (Heathcote et al., 1996).
We present a critical and contextualized review of the
gross anatomy, anatomical relations, and associated
musculature of these superstructures (Fig. 1), together
with the results of scanning electron microscope (SEM)
imaging of a single ancestral Chamorro cranium that
reveal novel topographic patterning of microstructures
on the cortical surface. English nomenclature, together
with acronyms faithful to the Latin terms, are used for
these traits, namely, tubercle on the TOT, PR, and TSP.
Collectively, these three are referred to as occipital
superstructures (OSSs), notwithstanding the frequent
extraoccipital (periasterionic) location of TSP. The primary objective of this study is to provide a foundation
for resolving the meaning of these enigmatic OSSs,
through consideration of what their functional anatomy
and microanatomy suggest about their genesis, development, and patterning.
In more marked degrees of development, OSSs appear
abruptly as well-circumscribed superstructures, with
surfaces that are smooth yet textured and penetrated by
vascular canals. Two of the OSSs (TOT and TSP) may
develop along or adjacent to the mendosal suture,
whereas one-third (PR) may arise inferior to this suture.
The mendosal suture demarcates the junction between
the membranous and endochondral developmental parts
of the occipital squamous. By the fifth fetal month, these
parts begin to fuse (Baker et al., 2005); however, the
suture may persist into adulthood as a hypostotic
sutural variant (Ossenberg, 1969, 2013, p 13–14). PR
superstructures have an exclusively endochondral origin.
TOT develops near the developmental interface marked
by the mendosal suture, whereas periasterionic TSP
develops in an ossification boundary zone proximal to
the lateral-most extensions of the mendosal suture,
where the parietals (of intramembranous origin) articulate with the (endochondrally formed) petromastoid portion of the temporals (see Davies and Coupland, 1967).
HISTORICAL BACKGROUND
Our collaboration began in 1989–1990, when three of
us (G.M.H., D.B.H., and B.E.A.) exchanged communications about markedly developed OSSs encountered in
our independent studies of archaeologically recovered
crania from the Mariana Islands (Figs. 2–4). Figure 2
illustrates marked expressions of two of the three traits
(TOT and PR) in a 45- to 55-year-old male (Bernice P.
Bishop Museum, No. 881) from the Taga Site, Tinian
(Heathcote et al., 2012a). The cranium of a middle-aged
male from Guam (#B-123), excavated from Gogna-Gun
Beach (Anderson, 1992), is shown in Figure 3. The most
striking morphological feature of this individual is a set
of large, pedunculated TSP located along the parietal–
mastoid suture, just anterior from asterion (Fig. 1). Figure 4 shows a 40- to 45-year-old female (Nansay-4),
recovered from the Achugao area of Saipan. Although
supraorbital development, nuchal crest, and mastoid
process size are equivocal with regard to sex, this individual’s subpubic angle and sciatic notch are strongly
female-like, and femoral and humeral head dimensions
are consistent with the latter assessment (Hanson,
1995). Although her periasterionic regions lack superstructure development, Nansay-4 has enormous pedunculated tubercles at the left and right TOT sites and also
bears markedly expressed PR, projecting downward
bilaterally from lateral continuations of the occipital
torus (OT).
Our initial (and false) impression that these superstructures had received little attention from previous
researchers, beyond nonspecific remarks about occipital
rugosity in some Oceanic crania, was based on the feedback during conference presentations (e.g., Anderson,
1992; Hanson, 1992; Heathcote et al., 1992), correspondences with colleagues, and examination of numerous
human anatomy texts and atlases, including those
known for coverage of morphological variation and
anomalies (Anson, 1963; Trotter and Peterson, 1966;
Anderson, 1983), as well as two compendia on human
CRANIAL SUPERSTRUCTURES IN MARIANA ISLANDERS
Fig. 1. Schematic drawing on left shows locations of three posterior
cranial superstructures in relation to muscle attachment sites and anatomic features discussed in text (after Fig. 12.14 in Aiello and Dean,
1990; used with the permission of Leslie Aiello). TOT, tubercles on the
1011
occipital torus; PR, retromastoid process; TSP, posterior supramastoid
tubercle. Illustration at right shows these superstructures on the posterior cranium of a 40- to 50-year-old male from the Gogna-Gun Beach
site, Guam (Burial No. 123).
Fig. 2. Skull, right lateral view, of a 40- to 50-year-old male from the
Taga Site, Tinian (Bernice Pauahi Bishop Museum, No. 881). Superstructure scores are TOT 5 3, PR 5 4, and TSP 5 2 (see Heathcote
et al., 1996).
anatomic variation (Bergman et al., 1988; Tountas and
Bergman, 1993). Furthermore, Kennedy’s (1989) wideranging review of purported skeletal markers of occupational stress made no mention of activity-induced
changes to the posterior cranium, and a comprehensive
work on epigenetic traits of the human skull made no
mention of TOT, only passing mention of TSP, and
although a weakly developed PR is illustrated (Hauser
and De Stefano, 1989, p 108), we failed initially to
Fig. 3. Cranium, baso-occipital view, of same individual illustrated in
Fig. 1. Left and right side superstructure scores are TOT 5 2/2, PR 5 2/2,
and TSP 5 4/4.
1012
HEATHCOTE ET AL.
Fig. 4. Cranium, left occipito-lateral view, of a 40- to 45-year-old female from Achuago, Saipan (Nansay-4). Left and right superstructure scores for TOT 5 4/4. Left side PR 5 3, and TSP 5 0.
appreciate its homology with much larger processes
observed on Mariana Islander crania.
Subsequent bibliographic research into primary literature revealed a number of pertinent studies, mostly in
non-English language publications from the mid to late
19th and early 20th centuries (e.g., Schaaffhausen,
1858; Joseph, 1873; Ecker, 1878; Hagen, 1880; Waldeyer,
1880, 1909, 1910; Le Double and Dubreuil-Chambardel,
1905; Matiegka, 1906; Schlaginhaufen, 1906; Michelsson, 1911; Passow, 1924; Hori, 1925; Hasebe, 1935), as
well as recent publications and reports (Jacob, 1967;
Arai, 1970; Hublin, 1978a; Pietrusewsky, 1990; Underwood, n.d.). Of these, Hasebe (1935) and Arai (1970) are
of greatest interest, given their attention to all three
OSSs and description and illustration of TOT, TSP, and
PR in Micronesian (including Mariana Islander) skulls.
The study of Hasebe included illustrations showing the
appearance of marked expressions of TOT and PR in living Micronesian men from Merir (Palau outlier), Ebon
(Ralik Chain of the Marshalls), “Guajelen” (Kwajalein in
the Marshalls), Pohnpei (Mokil), and Jaluit (Ralik Chain
of the Marshalls).
PREVIOUS STUDIES OF POSTERIOR
CRANIAL SUPERSTRUCTURES
Earlier literature on the morphology of the posterior
cranium, mostly written in German, features fairly consistent nomenclature for OSSs in modern humans; however, recent studies introduced a proliferation of
terminology. Concordances for older and newer nomenclature are provided below in discussions about the gross
morphology and anatomic relations of OSSs. We adapted
the scheme of Waldeyer (1880, 1909), who recognized
four OSSs as the most commonly encountered in modern
humans: OT; TSA and TSP; and PR. Studies that have
adopted our nomenclature and/or OSS scoring protocol
(Heathcote et al., 1996) include Douglas et al. (1997),
Pietrusewsky et al. (1997), Capasso et al. (1999),
CRANIAL SUPERSTRUCTURES IN MARIANA ISLANDERS
Valentin et al. (2005), Littleton and Kinaston (2008),
Weiss (2010), and Matisoo-Smith (2011).
Occipital Torus and Tubercles on the Occipital
Torus
Various aspects of the OT, including its morphology,
size variation, placement, and proposed homologies with
occipital crests in nonhuman primates, are discussed in
the older literature (e.g., Schaaffhausen, 1858; Joseph,
1873; Ecker, 1878; Hagen, 1880; Waldeyer, 1880, 1909;
Matiegka, 1906; Hori, 1925; Hasebe, 1935; Arai, 1970).
The OT is a marked transverse ridge on the squamous
part that, in sublime expression, characterizes Homo
erectus (sensu lato), and in structurally reduced form is
variably encountered in modern H. sapiens (Trotter and
Peterson, 1966; Lahr, 1994). It is considered present
when a plateau of bone, located between the superior
nuchal line (SNL) and highest nuchal line (HNL), forms
a transverse ridge across the posterior-most portion of
the occipital bone (Ecker, 1878; Waldeyer, 1880; Weidenreich, 1940).
TOT appear to represent focalized secondary superstructural developments on top of the OT. Perhaps the
first to publish on TOT was Ecker (1878), who noted
that bilateral tubercles were sometimes present on the
OT. These were named “supranuchal tubercles” by
Hasebe (1935), and this term is used by Hublin (1978a),
whereas Lahr (1995) prefers “Tubercle of Hasebe.” We do
not adopt these terms, because the former (and, by
extension, the latter) is a misnomer, for nonmarked TOT
developments occur at (not above) the level of the SNL
(Fig. 1). Although marked expressions of TOT extend
somewhat superior to the SNL, the term “supranuchal”
does not describe the full range of TOT morphological
expression.
Retromastoid Process
Early works on the PR include Le Double and
Dubreuil-Chambardel (1905), Schlaginhaufen (1906),
Waldeyer (1909), Hori (1925), and Hasebe (1935). The
PR (Fig. 1) appears as a variably raised tuberosity or
process at the insertion site of the m. obliquus capitis
superior (superior oblique muscle), where the superior
branch of the inferior nuchal line (INL) converges with
the lateral portion of the SNL. A variant expression of
the PR is a ridge of bone that extends from the most
inferior point of the PR and runs parallel to the occipito–mastoid suture (Waldeyer, 1909). The PR should
not be confused with weak bumps that may be present
along the INL, such as the tuberculum crurium, at the
bifurcation of the INL (Michelsson, 1911). Likewise, the
PR should not be confused with protuberances that can
develop higher along the crista asteriaca inferior (inferior asterial crest), as thickenings of the lateral portions
of the highest and superior nuchal lines, above the insertion site of the superior oblique muscle (Matiegka, 1906).
Waldeyer (1909) was skeptical about a functional
interpretation for PR, as he did not understand how the
small muscle that inserts at its location could produce a
large process. He illustrated dissections of deep and
superficial neck and shoulder muscles showing a set of
rather small PR anchoring small superior oblique
muscles and appears not to have considered muscular
1013
correlates of larger PRs. Waldeyer pondered a cultural
modification explanation for PR development, mentioning use of a wooden neck support/pillow by mid-19thcentury Fijians, and how it allegedly produced a
“scirrhus lump, (often) as large as a goose egg” on the
nape of the neck (Wilkes, 1845 in Waldeyer, 1909, p 15),
but did not pursue this association further, as Felix von
Luschan advised him that people who use wooden neck
supports generally rest with the side of their head, not
their neck, on such supports (Waldeyer, 1909, p 15).
Supramastoid Tubercles (TSA and TSP)
Waldeyer (1909, 1910) described two distinct round or
oblong tubercles, TSA and TSP, which may occur from
the region of the supramastoid crest and parietal notch
to the area surrounding asterion (see Planche V and
Figs. 1 and 3 in Hublin, 1978a). This region includes the
attachment sites of m. sternocleidomastoideus (sternocleidomastoid muscle [SCM]) and m. splenius capitis
(splenius capitis) and extends anteriorly to the posteriorand inferior-most point of attachment of the temporalis
muscle. The TSA is located at the posterior-most portion
of the supramastoid crest on the temporal bone. The
descriptive morphology of TSA is covered in the study by
Matiegka (1906), whereas the study by Jacob (1967) discusses variations. In developing our scoring system for
supramastoid tubercles (see Heathcote et al., 1996, p
287, 294), a much greater range of phenotypic expression was noted for TSP than for TSA. As a result of this
empirical finding, and in view of there being more published research on TSP, TSA was dropped from our
protocol.
The TSP is found in the vicinity of the parietal–mastoid suture and can be encountered on the temporal or
parietal bone, or both, and may involve a small portion
of the occipital at asterion (Fig. 1). We sometimes use
the term “periasterionic tubercles” as a descriptor (cf.
nomen) to refer to topographic variants of the TSP that
develop in proximity to asterion. Protuberant developments along the inferior asterial crest, situated inferior
to asterion on the occipital bone, are likely not occipital
variants of the TSP, as the former are thought to be
associated with aponeurotic attachments that mark the
SNL and highest nuchal lines (Matiegka, 1906, p 411).
When restricted to the parietal bone, the TSP is located
immediately anterior and superior to asterion, which is
why Haferland (1905) referred to this variation as the
processus asteriacus (asterionic process [AP]).
We agree with researchers who have considered the AP
to be a variation of the TSP (Matiegka, 1906; Schlaginhaufen, 1906; Passow, 1924; Hasebe, 1935). In contrast,
Jacob (1967) and Arai (1970) maintained that the TSP
occurs on the temporal bone, and Hauser and De Stefano
(1989, p 107) stated that its location is limited to the base
of the mastoid process of the temporal, anterior to the
occipito-mastoid suture. The claim that TSP can be found
at the midportion and posterior edge of the mastoid process (Waldeyer, 1909, 1910) is doubtful. Such (more inferiorly located) tubercles may be localized swellings along
the crista mastoidea (mastoid crest), a trait not systematically scored by us, although we noted that strong mastoid crest markings are regularly associated with
markedly developed TSP in crania from the Marianas.
Mastoid crests are associated with the SCM muscle and
1014
HEATHCOTE ET AL.
are characteristically well developed in Homo erectus
(sensu lato; Aiello and Dean, 1990). An anterior swelling
along the mastoid crest, the tuberculum mastoideum
anterius, has been identified as one of the four apomorphic characteristics of European Neanderthal skulls
(Hublin, 1978b) and is not homologous with the TSP.
Some authors have alleged that the AP is homologous
with the angular (or temporal) torus of the parietal. The
angular torus (AT), best known from the studies of
archaic hominins, is a ridged portion of the posterior
superior temporal line marking the attachment of the
posterior fibers of hypertrophied temporalis muscles and
their fascial covering (see Aiello and Dean, 1990, p 66–
67). In some Asian H. erectus, including crania from
Ngandong, Java (Wolpoff, 1999), the AT is located at the
mastoid angle of the parietal, superior to asterion (Weidenreich, 1943, 1951). Matiegka (1906), Waldeyer (1909),
and Hasebe (1935) considered the AP to be a variation of
the AT. However, we disagree, for we (G.M.H. and
V.J.S.) have examined modern Pacific crania with
weakly developed AT that co-occur with AP (viz. periasterionic TSP). In these cases, the AT is located well anterior of asterion, owing to the more forward placement of
the posterior fibers of the temporalis muscle in modern
humans versus archaic hominins (see Aiello and Dean,
1990, p 65).
ASSOCIATED MUSCULATURE
This section is informed by Davies and Coupland
(1967), Trotter and Peterson (1966), Crouch (1985), Shipman et al. (1985), O’Rahilly (1986), Romanes (1986),
Cartmill et al. (1987), Aiello and Dean (1990), Kreighbaum and Barthels (1990), and Rosse and GaddumRosse (1997). For the most part, these sources are in
essential agreement about origins, insertions, and
actions of muscles associated with TOT, PR, and TSP.
The studies that dispute or qualify the anatomical canon
are cited below.
Muscles Associated With the TOT Site
The semispinalis capitis muscle inserts between the
inferior and superior nuchal lines on the occipital bone
in a noncircumscribed region of the planum nuchae just
inferior to the TOT site. However, it appears that TOT
superstructures are not associated with the semispinalis
capitis in a functional sense. Fleshy fibers of this muscle
attach directly onto the periosteum, and such entheses
produce a smooth underlying bone surface with boundaries not well defined (Hems and Tillman, 2000; Benjamin et al., 2002).
In contrast, the enthesis for the origin of the upper
part of the trapezius muscle appears to be related functionally to TOT genesis and development. The bilateral
origin sites are located parasagitally along the SNL and,
if TOT is markedly expressed, on top of an OT (Fig. 1).
The upper trapezius assists in the extension and hyperextension of the neck, bends the neck toward the same
side, and draws the clavicle backward, in actions such
as pulling and rowing. Although often stated that the
trapezius has a direct role in elevating the scapula, a
dissection study of the fascicular anatomy of the trapezius disputes this. Johnson et al. (1994) demonstrated a
transverse orientation of the upper and middle trapezius
fibers, which is not consistent with a scapular elevation
function. Their study revealed that the nuchal portion of
the upper trapezius draws the clavicle backward or
medially and thus plays only an indirect role in moving
the scapula through the acromioclavicular joint. An overlooked action of the upper trapezius, involving the fascicle that attaches at the SNL (TOT site), is support for
the lateral clavicle and acromion of the scapula, for
example, when heavy weights are held by the hands,
with the arms down at the side (Luttgens and Wells,
1989). Although the fibers of the upper trapezius are
among the smallest and weakest of the trapezius fascicles, their oblique orientation give them the capacity to
exert compressive loads on the neck (Johnson et al.,
1994) when weights are so carried in the hands.
Muscle Associated With the PR Site
The superior oblique muscle is one of the four sets of
short suboccipital muscles, situated deeply at the base of
the neck. This muscle originates from tendinous fibers
on the upper surface of the transverse process of the
atlas and inserts onto the PR site on the occipital bone,
between the SNL and INL, lateral to the semispinalis
capitis and overlapping the insertion of the rectus capitis
posterior major (Fig. 1). Schlaginhaufen (1906) thought
that PR marked the site of a “fallen” splenius capitis
insertion; however, he was mistaken, as shown by Waldeyer (1909), who dissected and illustrated the superior
oblique muscle inserting at the PR site. The actions of
the superior oblique, together with the splenius capitis,
are bending the neck backward (when both act together)
and rotating it to the same side (when one acts alone).
Together with the rectus capitis posterior major and
minor, it serves as a postural muscle.
Although more superficial fascicles of the muscle may
insert directly at the PR site, a microdissection study
has shown that a “hidden” internal tendon (aponeurosis)
runs the course of the superior oblique (Kamibayashi
and Richmond, 1998). Thus, the insertion enthesis would
be at least partially fibrocartilagenous.
Muscles Associated With the TSP Site
Two muscles converge on the TSP site, the SCM,
sometimes referred to as the sternomastoid, and the
occipital part of the m. occipitofrontalis (OPO). The
OPO, one of the two scalp muscle groups, consists of
four bellies, two occipital and two frontal. The occipital
OPO originates from the HNL in the region of the mastoid angle of the parietal. Insertion is into the epicranial
aponeurosis, and its action is to pull the scalp backward.
As to whether the OPO could transmit sufficient loads
to have a role in the genesis of TSP superstructures, it
is pertinent that Bromage (unpublished data) has examined macaque brow ridge histology and has seen evidence of substantial connections of the OPO frontal
aponeurosis to the brow ridges; enough, he feels, to
strain the brow ridge considerably. Notwithstanding a
possible role of the OPO in TSP development, this superstructure appears to be primarily related to SCM activity, however.
Acting together, the SCM muscles draw the neck forward and raise it when the body is supine, and if the
neck is fixed, the SCM assists in raising the thorax in
CRANIAL SUPERSTRUCTURES IN MARIANA ISLANDERS
Fig. 5. SEM scans of Nansay-4, on the surface of a TOT and immediately adjacent to its base. A: Vermiculate morphology of the TOT
surface; such morphology suggests that the TOT surface may have
been covered with a fibrocartilagenous cap. B: A closer look at the
same surface reveals that the vermiculate pattern results from a series
of irregular-shaped ridges. C: A low-lying ridge and processes lie adjacent to the base of the TOT superstructure, shown at right, and an
1015
apparent incipient superstructure is shown in the center of this scan.
D: A closer look at this apparent microform shows a series of eminences rising up around foramina thought to be vascular canals. A wall to
a definitive vascular groove is shown (arrow). E: At greater magnification, anisotropic resorption bays are revealed along the wall and on
the floor of the vascular groove.
1016
HEATHCOTE ET AL.
Fig. 6. SEM scans on the occipital squamous surface of Nansay-4.
A: A representative low-magnification scan shows the very beginnings
of the vermiculate pattern observed on the TOT superstructures.
Apparent microforms of superstructures “rise up” in low-lying ridges,
particularly around presumed vascular canals. See this complex structure at the upper left corner. B: One of these microforms at greater
magnification, appearing as a semicircular formation with a trailing
forced respiration. When one SCM acts, it tilts the neck
toward the shoulder on the same side, and the face is
rotated to the opposite side. The SCM originates from
the front of the manubrium, below the clavicular notch,
and from the superior border of the medial third of the
clavicle. Most anatomy texts agree that the SCM inserts
via a thin aponeurosis onto the anterior border of the
mastoid process and the lateral portion of the SNL; however, Clemente (1985, p 457) dissented stating that the
SCM “inserts by a strong tendon into the lateral surface
of the mastoid process, and by a thin aponeurosis into
the lateral half of the superior nuchal line of the occipital bone.” Kamibayashi and Richmond (1998) documented that the sternomastoid portion of the SCM is
relatively thick, providing support for Clemente’s revision. By extension, this part of the SCM would not
insert at the TSP site via a thin aponeurosis.
ridge. To its left, a groove partially undercuts it and continues on to
penetrate the bone. C: A less magnified look at the squamous surface
shows the pattern observed in (B) to be quite widespread, practically
everywhere on the surface of the occipital of Nansay-4. D: Lowmagnification scans show that linear arrays of ridges are also consistently observed. These ridges presumably relate to inserting collagen
fiber bundles from muscles and tendons.
MICROANATOMY
A SEM imaging survey of the Nansay-4 OSS occipital
(Fig. 4) was conducted by T.G.B. All surfaces were
coated with gold to make them electrically conductive
and observed in secondary electron emission mode by a
LEO S440 SEM (Cambridge, UK) under conditions of
high vacuum, 10 kV accelerating voltage, 100 pA filament current, and relatively long-working distances to
permit enhanced fields of view. Observations of the
larger of the superstructures, the TOT, reveal a
vermiculate-like surface morphology (Fig. 5A). Normally,
such a surface would characterize underlying and relatively rapidly forming compacted cancellous bone. There
is no preferred orientation on the surface, which would
be expected if there had been muscular or tendinous collagenous insertions there. Thus, such a surface may
CRANIAL SUPERSTRUCTURES IN MARIANA ISLANDERS
have been covered with a fibrocartilagenous cap; however, in the absence of histological examination, we can
only speculate. A closer look at the same field illustrated
in Fig. 5A reveals the vermiculate pattern as a series of
irregular-shaped ridges (Fig. 5B). The smooth surfaces
are likely an artifact of abrasion exerted during diagenesis, preparation, and handling since deposition. The
foramina at the far lower left are vascular canals.
Frequently, low-lying ridges and processes emanate
from the base of the TOT (Fig. 5C). Along these ridges
are found incipient superstructures (OSS microforms?)
that give us a clue as to their formation. A closer look
reveals a series of eminences rising up around foramina
that, in this case, are vascular canals (Fig. 5D), on
which one can observe a resorptive wall on one of the
vascular floors (arrow). This occurs when vessels are
drifting, during growth, relative to the surrounding
bone. A yet closer look at the groove on the right reveals
resorption, as characterized by anisotropic resorption
bays, along the wall and partly down to the floor of the
groove (Fig. 5E). This is a very common observation
around the occipital, for example, on the TOT, adjacent
to the TOT, and elsewhere on the squamous occipital.
Evident remodeling around blood vessel canals is an
indication that vessels have changed their relative position during growth of the apparent microforms and/or
the growth of the individual. The latter possibility raises
the issue that these microscopic superstructures may
start to develop in juveniles. We cannot address this
question adequately, as we have not yet examined many
subadults. To date, the youngest individual for whom we
have recorded a moderate development of PR is a 15- to
16-year-old male (likely) Chamorro from Guam (Camp
Watkins Road Project, Burial No. 6B) of uncertain dating (PHRI, n.d.). The youngest individual we have seen
with moderate degrees of development for both TOT and
TSP is an approximately 18-year-old Chamorro male
from Guam (Gogna-Gun Beach, Burial No. B117), who
likely dates from the 10th to 15th centuries (Anderson,
1992).
Remarkably, SEM surveys of the occipital squamous
surface—beyond the boundaries of the TOT—reveal the
very beginnings of the vermiculate pattern (so readily
observed on the TOT surface), practically everywhere
(Fig. 6A). At their most incipient stage, small protrusions rise up and around low-lying ridges, particularly
around vascular canals, as mentioned above. A closer
look at one of these structures reveals a bleb of vermiculate bone, appearing as a semicircular mass with a trailing ridge (Fig. 6B). To the left of this mass, one can see
a vascular groove, which partially undercuts the edge,
traversing into the interior, and finally penetrating the
bone. This pattern can be found practically everywhere
on the squamous surface of the occipital bone (Fig. 6C).
Linear arrays of ridges are also consistently observed on
the surface, presumably in relation to inserting collagen
fiber bundles from muscles and tendinous sheaths (Fig.
6D). In these cases, from the least to the most developed,
it appears as if bone formation is concentrated between
bundles.
In summary, the analysis of SEM images of the
Nansay-4 occipital bone reveals a systemic effect on all
periosteal surfaces thus far examined. Vermiculate
ridges and mounds of bone matrix were formed and mineralized in association with the vasculature of this cra-
1017
nial bone. Rapid bone formation is typically associated
with a bone surface saturated with capillary vessels
(Bromage, 1984); however, the vessels associated with
the vermiculate ridges are substantially larger than
capillaries, indicating that the rate of bone formation
was deliberate and slow. The vermiculate bone formation
seems to not have been particularly related to specific
muscle or tendon insertions; however, because much of
the surface of this bone is covered in muscle and nuchal
ligament, the effect of numerous collagenous insertions
from the periosteum—too small to be observed by conventional SEM—cannot be ruled out as a mediator of
mechanical stress conduction to the bone. However, as
the associations of these peculiar bone structures are
with the vasculature passing through the bone cortex,
the microanatomical evidence suggests a systemic cause,
affecting the entire bone surface.
DISCUSSION
In over 30 years of conducting SEM surveys on
human and other primate crania, T.G.B. has never
before encountered such surface patterning. Such novel
and unexpected microanatomy, pointing to a systemic
effect in the expression of OSS, compounds their enigma,
given that their relationship to musculoskeletal stress
remains apparent at the macroscopic level. Activity
induction finds support from the spatial association of
OSSs with enthesis sites for the SCM, upper trapezius,
and superior oblique muscles and from recent investigations of OSS expression in relation to humeral robusticity, serving as a proxy for musculoskeletal exertion and
strength (Heathcote et al., 2012b, p 56). Heathcote et al.
(2012b) reported a significant positive correlation
(r 5 0.70; P < 0.003) between cumulative scores for OSS
development and indices of humeral robusticity in protohistoric Chamorros, whereas Weiss (2010) found a significant correlation (r 5 0.29; P < 0.05) between lesser
expressions of the same cranial muscle markers and
cross-sectional robusticity of humeri in California
Amerinds.
In our earlier OSS studies (see Capasso et al., 1999, p
11–12), TOT, PR, and TSP were conceptualized, more
straightforwardly than now, as cranially expressed musculoskeletal stress markers (MSMs; Hawkey and Merbs,
1995; Hawkey, 1998; Steen and Lane, 1998). MSMs are
thought to have potential for yielding interpretations of
chronic activity patterns, given the generally accepted
view that differential muscular activity leads to differential marking of bone at enthesis (osteotendinous junction) sites (Weiss, 2009; cf. Mariotti et al., 2004;
Schlecht, 2012; Foster et al., in press). Later, D.B.H.
took a lead role in our development of a more refined
multifactorial model of OSS activity induction (e.g.,
Heathcote et al., 2012b), according to which muscle
movement and consequent strain were viewed as proximate triggers of new fibrocartilage calcification at enthesis sites, with differential genetic predisposition,
interacting with strain and trauma, conceptualized as
the ultimate cause of OSS development.
Virtually all MSM studies have focused on the infracranial skeleton (cf. Weiss, 2010) and have been
informed by histological studies of long bones. Pioneer
studies of the latter (e.g., Benjamin et al., 1986) established two basic kinds of entheses, fibrous and
1018
HEATHCOTE ET AL.
fibrocartilagenous (Benjamin et al., 1986), and although
this dichotomy is now considered an oversimplification
(Benjamin et al., 2006; Villotte and Kn€
usel, 2013), the
following distinctions remain generally valid for the
infracranial skeleton: fibrous entheses, associated with
bone that ossifies intramembranously, are characterized
by direct attachment of fibrous connective tissue onto
bone or periosteum where cortical bone is relatively
thick, whereas fibrocartilagenous entheses, situated
near bone of endochondral origin, are associated with
thin cortices (Claudepierre and Voisin, 2005; Jurmain
and Villotte, 2010; Schlecht, 2012).
In more extreme degrees of expression, MSMs are
regarded as enthesopathies (Niepel and Sit’aj, 1979;
Mariotti et al., 2007), that is, lesions at tendon–bone (or
muscle–bone or ligament–bone) junctions. These lesions
manifest as “irregularities, rough patches, and bone projections or osteophytes” and are interpreted as developing in response to prolonged and excessive muscular
activity (Larsen, 1997, p 188). Kn€
usel (2000, p 387)
speaks of “enthesial activity-related change” that manifests either in bone deposition or resorption, the former
producing crests or spicules and the latter producing
sulcus-like excavations in cortical bone. The formulations of Larsen and Kn€
usel are consistent with the classification of MSMs by Hawkey and Merbs (1995) into (1)
robusticity markers, (2) stress lesions, and (3) ossification exostoses. Robusticity markers range in the expression from faint rugosities to sharp ridges or crests of
bone and are thought to reflect habitual muscle usage
connected with daily motor activities. Stress lesions are
considered to be the result of overactivity of muscles,
resulting in continuous microtrauma to attachment
sites, and are defined by pitting or furrowing into the
cortex, appearing as lytic lesions. They occur only at
insertion sites and are considered part of an activityrelated continuum, along with robusticity markers, as
evidenced by strong robusticity scores co-occurring with
weak stress lesion scores. In contrast, ossification exostoses are interpreted as being due to a macrotraumatic
episode, resulting in ligaments or muscle becoming ossified into new bone.
In our work with ancestral Chamorros, we have
encountered a few exuberantly developed OSSs that
have the appearance of robusticity markers grading into
stress lesions, but such changes could be the result of
normal surface remodeling related to the growth of the
OSSs. We have observed very few OSSs that manifest as
irregular, projecting osteophytes, thus a generalized
macrotraumatic origin of OSSs can be dismissed. Alternatively, conceptualizing an OSS as an MSM of the
robusticity marker variety is not without problems,
given that many OSSs do not look like they should, if
most anatomy texts are correct about the morphology of
soft tissue attachments at TOT, PR, and TSP sites
(Heathcote et al., 1995). There is reason to question
standard reference sources concerning normative morphology, however, as the factual bases of standard anatomy texts and atlases derive from dissection studies of
biogeographically biased (and non-Oceanic) cadaver collections and such sources often ignore or give little
attention to within- and between-population morphological variation.
Given our focus, the most problematic statements in
the standard literature are that the SCM inserts at the
TSP site and that the upper trapezius originates from
the TOT site, both by way of thin aponeuroses. It is
highly unlikely that such muscle–bone interfaces could
have been present in individuals whose skulls bear
markedly developed TSP and TOT superstructures.
Kamibayashi and Richmond’s (1998) microdissection
study is pertinent here, as they reported substantial
interindividual differences in the dimensions and crosssectional areas of human neck muscles, countering the
standard view that SCM necessarily attaches via thin
aponeuroses at the TSP region. Such findings, in the
grand tradition of 19th century studies on variations
and anomalies of human myology (e.g., Wood, 1868,
1870; Macalister, 1875; cf. Greiner et al., 2004), hardly
surprise us, for as biological anthropologists we expect
to find intragroup and intergroup diversity in anatomic
structures with complex etiologies.
Conceptualizing OSSs as developing at fibrocartilagenous entheses sites presents further appearance difficulties; however, this may be because what we think we
know of the osteological markings of such entheses is
derived from studies of the infracranial skeleton, almost
exclusively. Although the osteological signature of normal fibrocartilage entheses, located on thin-walled long
bone epiphyses or apophyses, is typically well circumscribed, smooth and avascular (Benjamin et al., 1986)
OSSs, situated on thick cranial cortex, have a different
topography. Although markedly expressed TOT, PR, and
TSP have an abrupt, well-defined morphology (Figs. 1–
4), their surfaces are penetrated by vascular canals and,
while generally smooth, are textured. What could
explain this contrast? One pertinent observation is that
subtendinous bursae may be found at fibrocartilagenous
entheses insertion sites and these are commonly associated with synovium. As synovium is proinflammatory
and highly vascular (Benjamin et al., 2002; Benjamin
and McGonagle, 2009), implications for osteological
appearance are apparent. In addition, entheses at OSS
sites could be “mixed,” as was found for the masseter
muscle insertion, where fibrocartilagenous junctions
appeared alongside periosteal and bony fibrous attachments (Hems and Tillmann, 2000). Furthermore, as
blood vessel growth is stimulated when tissue damage
occurs at fibrocartilagenous entheses (Benjamin et al.,
2007), and excessive biomechanical stress may hasten
vascularization of fibrocartilage, as well as calcification
and ossification of soft tissues at enthesis sites (Villotte
and Kn€
usel, 2013), these factors could well account for
the vascularity and textured surfaces of OSS at predominantly fibrocartilagenous enthesis sites.
Finally, we have considered a number of alternative
hypotheses on OSS development and meaning, unrelated
to mechanical induction, and will discuss them at length
in another paper. The most deserving of these are hereditary multiple exostoses (HMEs; Brannon and Fowler,
2001; Stieber and Dormans, 2005), benign fibro-osseous
lesion (BFOL; Lam et al., 2008; Sia et al., 2010), and
Ehlers-Danlos syndrome, Subtype IX (EDNINE; Sartoris
and Resnick, 1987; Yeowell and Pinnell, 1993). Consideration of such alternative etiologies has failed to find a
compelling candidate to account for the development and
patterning of OSSs; however, evaluation suffers from a
lack of SEM work carried out on bone lesions attributed
to HME, BFOL, EDNINE, or any other inherited connective tissue or bone matrix formation disorder. Indeed,
CRANIAL SUPERSTRUCTURES IN MARIANA ISLANDERS
SEM investigations of bone pathology, in general, are
rare (Schultz, 2001; cf. Sela, 1977).
CONCLUSIONS
Our review and novel SEM findings provide an
improved anatomical foundation for addressing the etiological, developmental, functional, and osteobiographical
meanings of OSSs in ancestral Chamorros and other
Oceanic peoples. At the gross anatomical level, the
abrupt and well-defined appearance of these superstructures (in marked expressions), coupled with vascularity
and smooth but textured surfaces, suggest that OSSs
develop at essentially fibrocartilagenous (but perhaps
“mixed”) enthesis sites, undergoing degenerative
changes in response to biomechanical stress. Covariation
of OSS expression and humeral robusticity is consistent
with upper body activity induction being a proximate
cause of these superstructures in genetically predisposed
individuals.
However, although our SEM work is based on a single
cranium and must be considered preliminary, unexpected findings demand questioning of, and amendments
to, any activity-induction model of OSS development.
The most interesting of the microanatomical findings is
that what we have been assuming to be discrete structures (the OSSs) appear to be relatively large components of a more generalized and systemic phenomenon.
There is a widespread distribution over the occipital surface of small structures (with a small size range) that
appear as microforms of OSSs (Figs. 6A–C). Further evidence in support of a systemic effect is that these apparent microforms are associated with vascular canals,
both on the surface of the OSS macrostructures (Fig.
5D) and on the surrounding squamous surface (Fig. 6A).
Further SEM survey work is needed to reconcile competing interpretations of OSS etiology. A key issue bearing on activity-induction model is this: if microtrauma to
entheses sites was involved in inducing TOT formation,
would the TOT surface observed under SEM look different than it does? At present, we cannot address this
question, for our preliminary SEM work cannot distinguish OSS development as a natural consequence of sustained or persistent muscular function or fibril
microtrauma at the entheses. An obstacle to such resolution is that there is a profound lack of knowledge about
tendon attachment morphology, namely, the microanatomy of collagenous insertions (Sharpey fibers) into hard
tissues. This deficiency needs to be resolved before
future research can determine whether the macroscopic
appearance of OSS sites relates significantly to prominent collagen fiber bundle insertions.
Future SEM studies should look elsewhere on other
OSS-bearing skulls, especially those with associated
infracranial skeletons, to examine the patterning of such
incipient outgrowths more comprehensively. In addition,
histological examinations should be carried out, as SEM
is most useful in combination with methods that reveal
the microstructure of bone underlying the surface
(Schultz, 2001). As such work is invasive, and permission to conduct it may not be granted, future studies
could use nondestructive means of visualizing subsurface microanatomy, such as confocal scanning optical
microscopy (Bromage et al., 2009). Further needs, in
testing the multifactorial mechanical induction model,
1019
include ancient DNA analysis of cultural peers who both
bear and do not bear markedly developed OSSs, as well
as conducting systematic macroscopic studies of the relationships among OSS and MSM expressions on the
infracranial skeleton. Individuals should be sampled
across a diachronic range inclusive of archaeological
assemblages that represent cultures with differing group
behavioral practices that may have literally embodied
different modalities of motor activity patterns. The full
dimensions of OSS meaning in late Pre-Contact and
Early Historic Chamorros, as well as in other Oceanic
populations, remain elusive; however, this work provides
a solid foundation on which to build further
investigations.
ACKNOWLEDGEMENTS
For translation of German works, the authors thank
Marion Reyes, Jurgen Carson-Greffe, and Peter Schuup,
and for permission to adapt a published figure of hers,
the authors thank Leslie Aiello. Various technical, bibliographic, editorial, and information-sharing assistance
was kindly provided by Kingbernam Bansil, Chris Bellessis, Arlene Cohen, Joanne Tarpley Crotts, Vincent
Diego, Moses Francisco, Yea Shin Huang, Diane Hawkey, Jean-Jacques Hublin, Rosalind Hunter-Anderson,
Rona Ikehara-Quebral, Marilyn Knudson, Marta Lahr,
Brian Millhoff, Michael Pietrusewsky, Tom Pinhey, J.R.
Ralphs, Frances Richmond, Susan Steen, Ann Stirland,
and the late Jane Underwood.
LITERATURE CITED
Aiello L, Dean C. 1990. An introduction to human evolutionary
anatomy. London: Academic Press.
Anderson BE. 1992. Preliminary report on the human skeletal
remains from the Gogna-Gun Beach Project, Tumon Bay, Guam.
In: Hanihara K, editor. International Symposium on Japanese as
a Member of the Asian and Pacific Populations. Kyoto: International Research Center for Japanese Studies. p 238–243.
Anderson JE, editor. 1983. Grant’s atlas of anatomy. 8th ed. Baltimore: Williams & Wilkins.
Anson BJ. 1963. An atlas of human anatomy. 2nd ed. Philadelphia,
PA: W.B. Saunders Company.
Arai S. 1970. Anthropometry of the Micronesians and eminences of
the occipital bones. Jikei Med J 17:95–112.
Baker BJ, Dupras TL, Tocheri MW. 2005. The osteology of infants
and children. College Station, TX: Texas A&M University Press.
Benjamin M, Evans EJ, Copp L. 1986. The histology of tendon
attachments to bone in man. J Anat 149:89–100.
Benjamin M, Kumai T, Milz S, Boszczyk BM, Boszcyk AA, Ralphs
JR. 2002. The skeletal attachment of tendons—tendon ‘entheses.’
Comp Biochem Physiol A 133:931–945.
Benjamin M, McGonagle D. 2009. Entheses: tendon and ligament
attachment sites. Scand J Med Sci Sports 19:320–327.
Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S.
2006. Where tendons and ligaments meet bone: attachment sites
(‘entheses’) in relation to exercise and/or mechanical load. J Anat
208:471–490.
Benjamin M, Toumi H, Suzuki D, Redman S, Emery P, McGonagle
D. 2007. Microdamage and altered vascularity at the enthesisbone interface provides an anatomic explanation for bone involvement in the HLA-B27-associated spondylarthritides and allied
disorders. Arthritis Rheum 56:224–233.
Bergman RA, Thompson SA, Afifi AK, Saadeh FA. 1988. Compendium of human anatomic variation: text, atlas, and world literature. Baltimore, MD: Urban & Schwarzenberg.
1020
HEATHCOTE ET AL.
Brannon RB, Fowler CB. 2001. Benign fibro-osseous lesions: a
review of current concepts. Adv Anat Pathol 8:126–143.
Bromage TG. 1984. Interpretation of scanning electron microscopic
images of abraded forming bone surfaces. Am J Phys Anthropol
64:161–178.
Bromage TG, Goldman HM, McFarlin SC, Perez-Ochoa A, Boyde A.
2009. Confocal scanning optical microscopy of a 3my Australopithecus afarensis Femur. Scanning 31:1–10.
Capasso L, Kennedy KAR, Wilczak CA. 1999. Atlas of occupational
markers on human remains. Journal of Paleontology, Monographic Publication 3. Teramo, Italy: Edigrafital S.P.A.
Cartmill M, Hylander WL, Shafland J. 1987. Human structure.
Cambridge: Harvard University Press.
Claudepierre P, Voisin M-C. 2005. The entheses: histology, pathology and pathophysiology. Joint Bone Spine 72:32–37.
Clemente CD, editor. 1985. Gray’s anatomy. 30th American Edition.
Baltimore, MD: Williams & Wilkins.
Crouch JE. 1985. Functional human anatomy. Philadelphia, PA:
Lea & Febiger.
Davies DV, Coupland RE, editors. 1967. Gray’s anatomy: descriptive
and applied. 34th edition. London: Longmans.
Douglas MT, Pietrusewsky M, Ikehara-Quebral RM. 1997. Skeletal
biology of Apurguan: a precontact Chamorro site on Guam. Am J
Phys Anthropol 104:291–313.
Ecker A. 1878. Uber den queren hinterhauptswulst (torus occipitalis transversus) am sch€
adel verschiedener ausserevop€
aischer
v€olker. Archiv f€
ur Anthropologie, V€
olkerforschung und Kolonialen
Kulturwandel 10:115–122.
Foster A, Buckley H, Tayles N. Using enthesis robusticity to infer
activity in the past: a review. J Archaeol Method Theory, in press.
Greiner TM, Bedford E, Walker RA. 2004. Variability in the human
M. spinalis capitis and cervicis: frequencies and definitions. Ann
Anat 186:185–191.
Haferland R. 1905. Einen sch€
adel mit einem processus asteriacus.
Zeitschrift f€
ur Ethnologie 37:207–208.
Hagen B. 1880. Uber einige bildungen an der hinterhauptsschuppe
des menschen. Beitraege Z€
ur Anthropologie und Urgeschichte
Bayerns 3:67–86.
Hanson DB. 1992. Neurodegenerative disease in the Western
Pacific: a post-contact phenomenon? Paper presented at the 25th
Annual CHACMOOL Conference, The archaeology of contact:
processes and consequences, Calgary, Alberta, November 12–15.
Hanson DB. 1995. Mortuary and skeletal analysis of human
remains from Achugao, Saipan. In: Butler B, editor. Archaeological investigations in the Achugao and Matansa area of Saipan,
Mariana Islands. Micronesian Archaeological Survey, Report 30. p
311–343.
Hasebe K. 1935. Knochenerhebungen in der schl€
afen- und nackengegend der sch€
adel der mikronesier. Anatomishche Institut des
Kaiserlische-Japanischen Universitat zu Sendai 17:1–9.
Hauser G, De Stefano GF. 1989. Epigenetic variants of the human
skull.
Stuttgart,
Germany:
E.
Schweizerbart’sche
Verlagsbuchhundlung.
Hawkey DE. 1998. Disability, compassion and the skeletal record:
using musculoskeletal stress markers (MSM) to construct an
osteobiography from Early New Mexico. Int J Osteoarchaeol 8:
326–340.
Hawkey DE, Merbs CF. 1995. Activity-induced musculoskeletal
stress markers (MSM) and subsistence strategy changes among
ancient Hudson Bay Eskimos. Int J Osteoarchaeol 5:324–338.
Heathcote GM, Anderson BE, Bromage TG, Collins S, Dean D,
Hanson DB, Kn€
usel C. 1992. Occipital superstructures in Pacific
Islanders: occupational markers? Paper presented at the 19th
Annual Meeting of the Paleopathology Association, Las Vegas,
March 31 and April 1.
Heathcote GM, Bansil KL, Sava VJ. 1996. An illustrated protocol
for scoring three posterior cranial superstructures which reach
remarkable size in Ancient Mariana Islanders. Micronesica 29:
281–297.
Heathcote GM, Diego VP, Ishida H, Sava VJ. 2012a. An osteobiography of a remarkable 16th–17th Century Chamorro Man from
Taga, Tinian. Micronesica 43:131–213.
Heathcote GM, Diego VP, Ishida H, Sava VJ. 2012b. Legendary
Chamorro strength: skeletal embodiment and the boundaries of
interpretation. In: Stodder ALW, Palkovich A, editors. The bioarchaeology of individuals. Gainesville, FL: University Press of
Florida. p 44–67.
Heathcote GM, Hanson DB, Anderson BE. 1995. Occipital and periasterionic superstructures on crania of Mariana Islanders. Poster
presentation for the symposium Prehistoric Human Skeletal Biology in Island Ecosystems: current status of bioarchaeological
research in the Marianas Archipelago, 64th Annual Meeting of
the American Association of Physical Anthropologists, Oakland,
March 28–April 1. Abstract published in Am J Phys Anthropol
Suppl 20, 1995, p 105.
Heathcote GM, Sava VJ, Hanson DB, Hublin J-J, Anderson BE.
Enigmatic cranial superstructures among Chamorro ancestors
from the Mariana Islands: population, geographic and temporal
variation. Forthcoming.
Hems T, Tillmann B. 2000. Tendon entheses of the human masticatory muscles. Anat Embryol 202:201–208.
€
Hori T. 1925. Uber
die anomalien des hinterhauptbeines. Folia Anat
Jpn 3:291–312.
Hublin J-J. 1978a. Le torus occipital transverse et les structures
associ
ees: evolution dans le genre Homo. 3d cycle Thesis. Paris:
Universit
e Pierre et Marie Curie. Vol. II.
Hublin J-J. 1978b. Quelques caractères apomorphes du cr^
ane
n
eandertalien et leur interpr
etation phylog
en
etique. Comptes
Rendus de l’Acad
emie des Sciences Paris, tome 287, s
erie D: 923–
926.
Jacob T. 1967. The morphologic variations of the supramastoid crest
and tubercles. Anthropologica 9:59–72.
Johnson G, Bogduk N, Nowitzke A, House D. 1994. Anatomy and
actions of the trapezius. Clin Biomech 9:44–50.
Joseph G. 1873. Morphologische studien am kopfskelet des menschen und der wirbelthiere. Breslau: W.G. Korn.
Jurmain R, Villotte S. 2010. Terminology. Entheses in medical literature and physical anthropology: a brief review. Document published online on 4th February following the Workshop in
Musculoskeletal Stress Markers (MSM): limitations and achievement in the reconstruction of past activity patterns, University of
Coimbra, Portugal. [Consulted on 11th June, 2013]. Available
from: http://www.uc.pt/en/cia/msm/MSM_terminology3.
Kamibayashi LK, Richmond FJR. 1998. Morphometry of human
neck muscles. Spine 23:1314–1323.
Kennedy KAR. 1989. Skeletal markers of occupational stress. In:
Işcan MY, Kennedy KAR, editors. Reconstruction of life from the
skeleton. New York: Alan R. Liss. p 129–160.
Kn€
usel C. 2000. Bone adaptation and its relationship to physical
activity in the past. In: Cox M, Mays S, editors. Human osteology
in archaeology and forensic science. London: Greenwich Medical
Media Ltd. p 381–401.
Kreighbaum E, Barthels KM. 1990. Biomechanics: a qualitative
approach for studying human movement. New York: Macmillan.
Lahr MM. 1994. The multiregional model of modern human origins:
a reassessment of its morphological basis. J Hum Evol 26:23–56.
Lahr MM. 1995. Patterns of modern human diversification: implications for Amerindian origins. Ybk Phys Anthropol 38:163–198.
Lam SY, Ramli MN, Harichandran D, Sia SF, Pailoor J. 2008. Ossifying fibroma of the occipital bone—a case report and literature
review. Eur J Radiol Extra 67:19–23.
Larsen CS. 1997. Bioarchaeology: interpreting behavior from the
human skeleton. Cambridge: Cambridge University Press.
Le Double AF, Dubrueuil-Chambardel L. 1905. Note sur le processus retro-mastoideus. Comptes Rendus de l’Associations des Anatomistes, 7th Session: 177–178.
Littleton J, Kinaston R. 2008. Ancestry, age, sex and stature: identification in a diverse space. In: Oxenham M, editor. Forensic
approaches to death, disaster and abuse. Brisbane: Australian
Academic Press. p 155–176.
Luttgens K, Wells KF. 1989. Kinesiology: scientific basis of human
motion. 7th ed. Dubuque, Iowa: W.C. Brown.
Macalister A. 1875. Additional observations on muscular anomalies
in human anatomy (third series), with a catalogue of the principal
CRANIAL SUPERSTRUCTURES IN MARIANA ISLANDERS
muscular variations hitherto published. Trans R Irish Acad 25:1–
130.
Mariotti V, Facchini F, Balcastro MG. 2004. Enthesopathies—proposal of a standardized scoring method and applications. Coll
Antropol 28:145–159.
Mariotti V, Facchini F, Belcastro MG. 2007. The study of entheses:
proposal of a standardized scoring method for twenty-three entheses of the postcranial skeleton. Coll Antropol 31:291–313.
€
Matiegka H. 1906. Uber
die an kammbildungen erinnernden merkmale des menschlichen sch€
adels. Sitzungsberichte der
Mathematisch-Naturwissenschaftlichen Klasse, Bd. CXV. Abt. III:
349–431.
Matisoo-Smith E. 2011. Human biological evidence for Polynesian
contacts with the Americas. In: Jones T, Storey A, Matisoo-Smith
E, Ramırez-Aliaga J, editors. Polynesians in America: preColumbian contacts with the New World. Lanham, Maryland:
AltaMira Press. p 201–214.
Michelsson G. 1911. Ein sch€
adel mit processus retromastoideus und
mit verminderung der zahl der z€
ahne. Anat Anze—Jena 39:667–
670.
Moore DR. 2002. Guam’s prehistoric pottery and its chronological
sequence. Prepared for the Department of the Navy, Pacific Division, Pearl Harbor, Hawaii. Micronesian Archaeological Research
Services, Guam.
1979. Enthesopathy. Clin Rheum Dis 5:857–
Niepel GA, Sit’aj S.
872.
O’Rahilly R. 1986. Gardner–Gray–O’Rahilly anatomy: a regional
study of human structure. 5th ed. Philadelphia, PA: W.B. Saunders Company.
Ossenberg NS. 1969. Discontinuous morphological variation in the
human cranium. Ph.D. Thesis. Toronto, ON: University of
Toronto.
Ossenberg NS. 2013. Cranial nonmetric trait database user guide.
Kingston, ON: Data and Government Information Centre,
Queen’s University Library. Available at: Cranial Nonmetric
Traits Database. [Consulted on 3rd June, 2013]. Available from:
http://library.queensu.ca/webdoc/ssdc/cntd.
Passow A. 1924. H€
ockerbildung am schl€
afenbein und in seiner
umgebung. Anatomie, Physiologie und Therapie des Ohres der
Nase und des Halsen 20:184–190.
PHRI. n.d. Project #757, currently unfunded. No work in progress.
Paul H. Rosendahl Incorporated, Maite, Guam. Collection and
files transferred to the Guam Museum.
Pietrusewsky M. 1990. The physical anthropology of Micronesia: a
brief overview. Micronesica Supplement 2:317–322.
Pietrusewsky M, Hunt TL, Ikehara-Quebral RM. 1997. A Lapitaassociated skeleton from Waya Island, Fiji. Micronesica 30:355–
388.
Romanes GJ. 1986. Cunningham’s manual of practical anatomy.
15th ed. Vol. III: Head and neck and brain. Oxford: Oxford University Press.
Rosse C, Gaddum-Rosse P. 1997. Hollinshead’s textbook of anatomy.
5th edition. Philadelphia, PA: Lippincott-Raven Publishers.
Sartoris DJ, Resnick D. 1987. The horn: a pathognomonic feature of
paediatric bone dysplasias. Aust Paediatr J 23:347–349.
€ltesten rassensch€
Schaaffhausen H. 1858. Zur kenntniss der a
adel.
M€
uller’s Archiv f€
ur Anatomie, Physiologie und wissenschaftliche
Medicin 25:453–478.
€
Schlaginhaufen O. 1906. Uber
eine sch€
adelserie von den Marianen.
Jahrbuch der St. Gallishchen Naturwissenschaftlichen Gesellschaft f€
ur das Vereinsjahr 1905:454–509.
1021
Schlecht SH. 2012. Understanding entheses: bridging the gap
between clinical and anthropological perspectives. Anat Rec 295:
1239–1251.
Schultz M. 2001. Paleohistopathology of bone: a new approach to
the study of ancient diseases. Ybk Phys Anthropol 44:106–147.
Sela J. 1977. Bone remodeling in pathologic conditions: a scanning
electron microscopic study. Calcif Tissue Res 23:229–234.
Shipman P, Walker A, Bichell D. 1985. The human skeleton. Cambridge: Harvard University Press.
Sia SF, Davidson AS, Soper JR, Gerarchi P, Bonar SF. 2010. Protuberant fibro-osseous lesion of the temporal bone: “Bullough
Lesion”. Am J Surg Pathol 34:1217–1223.
Steen SL, Lane RW. 1998. Evaluation of habitual activities among
two Alaskan Eskimo populations based on musculoskeletal stress
markers. Int J Osteoarchaeol 8:341–353.
Stieber JR, Dormans JP. 2005. Manifestations of hereditary multiple exostoses. J Am Acad Orthop Surg 13:110–120.
Tountas CP, Bergman RA. 1993. Anatomic variations of the upper
extremity. New York: Churchill Livingstone.
Trotter M, Peterson RR. 1966. Osteology. In: Anson BJ, editor. Morris’s human anatomy. Toronto: McGraw-Hill. p 133–315.
Underwood JH. n.d. Report on a preliminary examination of the
skeletal remains excavated on Guam, Mariana Islands. Manuscript on file, Department of Anthropology, Field Museum of Natural History, Chicago.
Valentin F, Shing R, Spriggs M. 2005. Des restes humains dat
es du
d
ebut de la p
eriode de Mangaasi (2400–1800 BP) d
ecouverts a
Mangaliliu (Efate, Vanuatu). Comptes Rendus Palevol 4:420–427.
Villotte S, Kn€
usel CJ. 2013. Understanding entheseal changes: definition and life course changes. Int J Osteoarchaeol 23:135–146.
€ ber die squama ossis occipitis
Waldeyer W. 1880. Bemerkungen u
mit besonderer ber€
ucksichtigung des “torus occipitalis.” Archiv
f€
ur Anthropologie 12:453–461.
Waldeyer W. 1909. Der processus retromastoideus. Abhandlung der
K€
oniglich Preussischen Akademie der Wissenschaften. Phys Math
Klasse 1909:1–32.
€ ber den processus retWaldeyer W. 1910. Weitere untersuchungen u
romastoideus. Zeitschrift f€
ur Ethnologie 42:316–317.
Weidenreich F. 1940. The torus occipitalis and related structures
and their transformations in the course of human evolution. Bull
Geol Surv China 19:480–558.
Weidenreich F. 1943. The skull of Sinanthropus pekinensis; a comparative study on a primitive hominid skull. Paleontologia Sinica,
New Series D, No. 10.
Weidenreich F. 1951. Morphology of solo man. New York: Anthropological Papers of the American Museum of Natural History. Vol.:
43, Part 3.
Weiss E. 2009. Bioarchaeological science: what we have learned from
human skeletal remains. New York: Nova Science Publishers.
Weiss E. 2010. Cranial muscle markers: a preliminary examination
of size, sex, and age effects. Homo. J Comp Hum Biol 61:48–58.
Wolpoff MH. 1999. Paleoanthropology. 2nd ed. New York: McGrawHill.
Wood J. 1868. Variations in human myology observed during the
Winter Session of 1867–68 at King’s College, London. Proc R Soc
Lond 16:483–525.
Wood J. 1870. On a group of varieties of the muscles of the human
neck, shoulder, and chest, with their transitional forms and homologies in the Mammalia. Philos Trans R Soc Lond 160:83–116.
Yeowell HN, Pinnell SR. 1993. The Ehlers-Danlos syndromes.
Semin Dermatol 12:229–240.